Conservation Genetics

, Volume 11, Issue 5, pp 1899–1910 | Cite as

Strategies for the retention of high genetic variability in European flat oyster (Ostrea edulis) restoration programmes

  • Delphine Lallias
  • Pierre Boudry
  • Sylvie Lapègue
  • Jon W. King
  • Andy R. Beaumont
Research Article


The native European flat oyster Ostrea edulis is listed in the OSPAR Convention for the Protection of the Marine Environment of the North-East Atlantic (species and habitat protection) and in the UK Biodiversity Action Plan. Once extremely abundant in the nineteenth century, European stocks of O. edulis have declined during the twentieth century to rare, small, localised populations due to overexploitation, habitat degradation and, most recently, the parasitic disease bonamiosis. Selective breeding programmes for resistance to bonamiosis have been initiated in France and Ireland. High genetic diversity and bonamiosis-resistance would be important features of any sustainable restoration programmes for O. edulis. Oysters were sampled across Europe from four hatchery sources, four pond-cultured sources and four wild, but managed fisheries and were genotyped at five microsatellite loci. Hatchery-produced populations from small numbers of broodstock showed a significant loss of genetic diversity relative to wild populations and pedigree reconstruction revealed that they were each composed of a single large full-sib family and several small full-sib families. This extremely low effective population size highlights the variance in reproductive success among the potential breeders. Pond-cultured oysters were intermediate in genetic diversity and effective population size between hatchery and wild populations. Controlled hatchery production allows the development of bonamiosis-resistant strains, but at the expense of genetic diversity. Large scale pond culture on the other hand can provide a good level of genetic diversity. A mixture of these two approaches is required to ensure a healthy and sustainable restoration programme for O. edulis in Europe.


Restoration programme Ostrea edulis Genetic variation Pedigree reconstruction 


  1. Appleyard SA, Ward RD (2006) Genetic diversity and effective population size in mass selection lines of Pacific oyster (Crassostrea gigas). Aquaculture 254:148–159CrossRefGoogle Scholar
  2. Arnold WS (2008) Application of larval release for restocking and stock enhancement of coastal marine bivalve populations. Rev Fish Sci 16:65–71CrossRefGoogle Scholar
  3. Arnold WS, Marelli DC, Parker M, Hoffman P, Frischer M, Scarpa J (2002) Enhancing hard clam (Mercenaria spp.) population density in the Indian River Lagoon, Florida: a comparison of strategies to maintain the commercial fishery. J Shellfish Res 21:659–672Google Scholar
  4. Arnold WS, Blake NJ, Harrison MM, Marelli DC, Parker ML, Peters SC, Sweat DE (2005) Restoration of bay scallop (Argopecten irradians (Lamarck)) populations in Florida coastal waters: planting techniques and the growth, mortality and reproductive development of planted scallops. J Shellfish Res 24:883–904Google Scholar
  5. Beaumont AR, Trebano Garcia M, Honig S, Low P (2006) Genetics of Scottish populations of the native oyster, Ostrea edulis: gene flow, human intervention and conservation. Aquat Living Resour 19:389–402CrossRefGoogle Scholar
  6. Beebee TJC (2009) A comparison of single-sample effective size estimators using empirical toad (Bufo calamita) population data: genetic compensation and population size-genetic diversity correlations. Mol Ecol 18:4790–4797CrossRefPubMedGoogle Scholar
  7. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (1996–2001) GENETIX 4.02, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, MontpellierGoogle Scholar
  8. Bierne N, Launey S, Naciri-Graven Y, Bonhomme F (1998) Early effect of inbreeding as revealed by microsatellite analyses on Ostrea edulis larvae. Genetics 148:1893–1906PubMedGoogle Scholar
  9. Boudry P, Collet B, Cornette F, Hervouet V, Bonhomme F (2002) High variance in reproductive success of the Pacific oyster (Crassostrea gigas, Thunberg) revealed by microsatellite-based parentage analysis of multifactorial crosses. Aquaculture 204:283–296CrossRefGoogle Scholar
  10. Bouza C, Sanchez L, Martinez P (1997) Gene diversity analysis in natural populations and cultured stocks of turbot (Scophthalmus maximus L.). Anim Genet 28:28–36CrossRefGoogle Scholar
  11. Brumbaugh RD, Sorabella LA, Garcia CO, Goldsborough WJ, Wesson JA (2000) Making a case for community-based oyster restoration: an example from Hampton Roads, Virginia, U.S.A. J Shellfish Res 19:467–472Google Scholar
  12. Chícharo L, Chícharo MA (2001) Effects of environmental conditions on planktonic abundances, benthic recruitment and growth rates of the bivalve mollusc Ruditapes decussatus in a Portuguese coastal lagoon. Fish Res 53:235–250CrossRefGoogle Scholar
  13. Culloty SC, Cronin MA, Mulcahy MF (2004) Potential resistance of a number of populations of the oyster Ostrea edulis to the parasite Bonamia ostreae. Aquaculture 237:41–58CrossRefGoogle Scholar
  14. da Silva PM, Fuentes J, Villalba A (2005) Growth, mortality and disease susceptibility of oyster Ostrea edulis families obtained from brood stocks of different geographical origins, through on-growing in the Ría de Arousa (Galicia, NW Spain). Mar Biol 147:965–977CrossRefGoogle Scholar
  15. Drinkwaard A (1999) Introductions and developments of oysters in the North Sea area: a review. Helgol Meeresunters 52:301–308CrossRefGoogle Scholar
  16. El Mousadik A, Petit RJ (1996) High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L.) Skeels] endemic to Morocco. Theor Appl Genet 92:832–839CrossRefGoogle Scholar
  17. Foighil DO (1989) Role of spermatozeugmata in the spawning ecology of the brooding oyster Ostrea edulis. Gamete Res 24:219–228CrossRefPubMedGoogle Scholar
  18. Gaffney PM (2006) The role of genetics in shellfish restoration. Aquat Living Resour 19:277–282CrossRefGoogle Scholar
  19. Gaffney PM, Davis CV, Hawes RO (1992) Assessment of drift and selection in hatchery populations of oysters (Crassostrea virginica). Aquaculture 105:1–20CrossRefGoogle Scholar
  20. Gathorne-Hardy A, Hugh-Jones T (2004) Spat collection in native oyster ponds. Shellfish News 17:6–9Google Scholar
  21. Gosling EM (1982) Genetic variability in hatchery-produced Pacific oysters (Crassostrea gigas Thunberg). Aquaculture 26:273–287CrossRefGoogle Scholar
  22. Goudet J (1995) FSTAT (vers. 1.2): a computer program to calculate F-statistics. J Hered 86:485–486Google Scholar
  23. Guillemin ML, Faugeron S, Destombe C, Viard F, Correa JA, Valero M (2008) Genetic variation in wild and cultivated populations of the haploid-diploid red alga Gracilaria chilensis: how farming practices favor asexual reproduction and heterozygosity. Evolution 62:1500–1519CrossRefPubMedGoogle Scholar
  24. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Palaeontological statistics software package for education and data analysis. Palaeontol Electronica 4:9Google Scholar
  25. Hara M, Sekino M (2007) Genetic differences between hatchery stocks and natural populations in Pacific abalone (Haliotis discus) estimated using microsatellite DNA markers. Mar Biotechnol 9:74–81CrossRefPubMedGoogle Scholar
  26. Hare MP, Allen SK, Bloomer P, Camara MD, Carnegie RB, Murfree J, Luckenbach M, Meritt D, Morrison C, Paynter K, Reece KS, Rose CG (2006) A genetic test for recruitment enhancement in Chesapeake Bay oysters, Crassostrea virginica, after population supplementation with a disease tolerant strain. Conserv Genet 7:717–734CrossRefGoogle Scholar
  27. Hedgecock D, Sly F (1990) Genetic drift and effective population sizes of hatchery-propagated stocks of the Pacific oyster, Crassostrea gigas. Aquaculture 88:21–38CrossRefGoogle Scholar
  28. Hedgecock D, Chow V, Waples RS (1992) Effective population numbers of shellfish broodstocks estimated from temporal variance in allelic frequencies. Aquaculture 108:215–232CrossRefGoogle Scholar
  29. Hedgecock D, Launey S, Pudovkin AI, Naciri Y, Lapègue S, Bonhomme F (2007) Small effective number of parents (Nb) inferred for a naturally spawned cohort of juvenile European flat oysters Ostrea edulis. Mar Biol 150:1173–1182CrossRefGoogle Scholar
  30. Herbinger CM, O’Reilly PT, Verspoor E (2006) Unravelling first-generation pedigrees in wild endangered salmon populations using molecular genetic markers. Mol Ecol 15:2261–2275CrossRefPubMedGoogle Scholar
  31. Hill WG (1981) Estimation of effective population size from data on linkage disequilibrium. Genet Res 38:209–216CrossRefGoogle Scholar
  32. Hugh-Jones T (2003) The Loch Ryan native oyster fishery. Shellfish News 15:17–18Google Scholar
  33. Kirkland DW, Platt Bradbury J, Dean WE (1983) The heliothermic lake—a direct method of collecting and storing solar energy. Arch Hydrobiol 65:1–60Google Scholar
  34. Laing I, Walker P, Areal F (2005) A feasibility study of the native oyster (Ostrea edulis) stock regeneration in the United Kingdom (CARD Project Report FC1016). Available via DIALOG,
  35. Laing I, Walker P, Areal F (2006) Return of the native—is European oyster (Ostrea edulis) stock restoration in the UK feasible? Aquat Living Resour 19:283–287CrossRefGoogle Scholar
  36. Lallias D, Beaumont AR, Haley CS, Boudry P, Heurtebise S, Lapègue S (2007) A first-generation genetic linkage map of the European flat oyster Ostrea edulis (L.) based on AFLP and microsatellite markers. Anim Genet 38:560–568CrossRefPubMedGoogle Scholar
  37. Lallias D, Gomez-Raya L, Haley C, Arzul I, Heurtebise S, Beaumont A, Boudry P, Lapègue S (2009) Combining two-stage testing and interval mapping strategies to detect QTL for resistance to bonamiosis in the European flat oyster Ostrea edulis. Mar Biotechnol 11:570–584CrossRefPubMedGoogle Scholar
  38. Launey S, Hedgecock D (2001) High genetic load in the Pacific oyster Crassostrea gigas. Genetics 159:255–265PubMedGoogle Scholar
  39. Launey S, Barre M, Gerard A, Naciri-Graven Y (2001) Population bottleneck and effective size in Bonamia ostreae-resistant populations of Ostrea edulis as inferred by microsatellite markers. Genet Res 78:259–270CrossRefPubMedGoogle Scholar
  40. Launey S, Ledu C, Boudry P, Bonhomme F, Naciri-Graven Y (2002) Geographic structure in the European flat oyster (Ostrea edulis L.) as revealed by microsatellite polymorphism. J Hered 93:331–351CrossRefPubMedGoogle Scholar
  41. Li G, Hedgecock D (1998) Genetic heterogeneity, detected by PCR-SSCP, among samples of larval Pacific oysters (Crassostrea gigas) supports the hypothesis of large variance in reproductive success. Can J Fish Aquat Sci 55:1025–1033CrossRefGoogle Scholar
  42. Lind CE, Evans BS, Knauer J, Taylor JJU, Jerry DR (2009) Decreased genetic diversity and a reduced effective population size in cultured silver-lipped pearl oysters (Pinctada maxima). Aquaculture 286:12–19CrossRefGoogle Scholar
  43. Liu Y, Chen S, Li B (2005) Assessing the genetic structure of three Japanese flounder (Paralichthys olivaceus) stocks by microsatellite markers. Aquaculture 243:103–111CrossRefGoogle Scholar
  44. Luikart G, Cornuet JM (1999) Estimating the effective number of breeders from heterozygote excess in progeny. Genetics 151:1211–1216PubMedGoogle Scholar
  45. Lundrigan TA, Reist JD, Ferguson MM (2005) Microsatellite genetic variation within and among Arctic charr (Salvelinus alpinus) from aquaculture and natural populations in North America. Aquaculture 244:63–75CrossRefGoogle Scholar
  46. Machado-Schiaffino G, Dopico E, Garcia-Vazquez E (2007) Genetic variation losses in Atlantic salmon stocks created for supportive breeding. Aquaculture 264:59–65CrossRefGoogle Scholar
  47. MacKenzie CL, Burrel VG, Rosefield A, Hobart WL (1997) The history, present condition, and future of the molluscan fisheries of north and central America and Europe. National Marine Fisheries Service, Washington, DCGoogle Scholar
  48. Mann R (2000) Restoring the oyster reef communities in the Chesapeake bay: a commentary. J Shellfish Res 19:335–339Google Scholar
  49. McCay DPF, Peterson CH, DeAlteris JT, Catena J (2003) Restoration that targets function as opposed to structure: replacing lost bivalve production and filtration. Mar Ecol Prog Ser 264:197–212CrossRefGoogle Scholar
  50. Milbury C, Meritt D, Newell R, Gaffney P (2004) Mitochondrial DNA markers allow monitoring of oyster stock enhancement in the Chesapeake Bay. Mar Biol 145:351–359CrossRefGoogle Scholar
  51. Morgan TS, Rogers AD, Iyengar A (2000) Novel microsatellite markers for the European oyster Ostrea edulis. Mol Ecol 9:495–497CrossRefPubMedGoogle Scholar
  52. Naciri Y, Vigouroux Y, Dallas J, Desmarais E, Delsert C, Bonhomme F (1995) Identification and inheritance of (GA/TC)n and (AC/GT)n repeats in the European flat oyster Ostrea edulis (L.). Mol Mar Biol Biotechnol 4:83–89PubMedGoogle Scholar
  53. Naciri-Graven Y, Martin A-G, Baud J-P, Renault T, Gerard A (1998) Selecting the flat oyster Ostrea edulis (L.) for survival when infected with the parasite Bonamia ostreae. J Exp Mar Biol Ecol 224:91–107CrossRefGoogle Scholar
  54. Naciri-Graven Y, Launey S, Lebayon N, Gerard A, Baud JP (2000) Influence of parentage upon growth in Ostrea edulis: evidence for inbreeding depression. Genet Res 76:159–168CrossRefPubMedGoogle Scholar
  55. Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590PubMedGoogle Scholar
  56. Pullin AS, Knight TM (2009) Doing more good than harm—building an evidence-base for conservation and environmental management. Biol Conserv 142:931–934CrossRefGoogle Scholar
  57. Ryman N, Laikre L (1991) Effects of supportive breeding on the genetically effective population size. Conserv Biol 5:325–329CrossRefGoogle Scholar
  58. Saavedra C (1997) Low effective sizes in hatchery populations of the European oyster (Ostrea edulis): implications for the management of genetic resources. J Shellfish Res 16:441–446Google Scholar
  59. Saavedra C, Guerra A (1996) Allozyme heterozygosity, founder effect and fitness traits in a cultivated population of the European oyster, Ostrea edulis. Aquaculture 139:203–224CrossRefGoogle Scholar
  60. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring HarbourGoogle Scholar
  61. Sobolewska H, Beaumont AR (2005) Genetic variation at microsatellite loci in northern populations of the European flat oyster (Ostrea edulis). J Mar Biol Assoc UK 85:955–960CrossRefGoogle Scholar
  62. Sobolewska H, Beaumont AR, Hamilton A (2001) Dinucleotide microsatellites isolated from the European flat oyster, Ostrea edulis. Mol Ecol Notes 1:79–80CrossRefGoogle Scholar
  63. Soulé ME (1976) Allozyme variation, its determinants in space and time. In: Ayala FJ (ed) Molecular evolution. Sinauer Associates, Sunderland, pp 46–59Google Scholar
  64. Taris N, Ernande B, McCombie H, Boudry P (2006) Phenotypic and genetic consequences of size selection at the larval stage in the Pacific oyster (Crassostrea gigas). J Exp Mar Biol Ecol 333:147–158CrossRefGoogle Scholar
  65. Taris N, Batista FM, Boudry P (2007) Evidence of response to unintentional selection for faster development and inbreeding depression in Crassostrea gigas larvae. Aquaculture 272:S69–S79CrossRefGoogle Scholar
  66. Wang J (2009) A new method for estimating effective population sizes from a single sample of multilocus genotypes. Mol Ecol 18:2148–2164CrossRefPubMedGoogle Scholar
  67. Waples RS, Do C (2008) LDNE: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Resour 8:753–756CrossRefGoogle Scholar
  68. Waples RS, Do C (2009) Linkage disequilibrium estimates of contemporary N e using highly variable genetic markers: a largely untapped resource for applied conservation and evolution. Evol Appl. doi:10.1111/j.1752-4571.2009.00104.x
  69. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  70. Wilbur AE, Seyoum S, Bert TM, Arnold WS (2005) A genetic assessment of bay scallop (Argopecten irradians) restoration efforts in Florida’s Gulf of Mexico Coastal Waters (USA). Conserv Genet 6:111–122CrossRefGoogle Scholar
  71. Wright S (1931) Evolution in Mendelian populations. Genetics 16:97–159PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Delphine Lallias
    • 1
    • 2
  • Pierre Boudry
    • 3
  • Sylvie Lapègue
    • 4
  • Jon W. King
    • 2
  • Andy R. Beaumont
    • 1
    • 2
  1. 1.School of Ocean Sciences, College of Natural SciencesBangor UniversityMenai Bridge, AngleseyUK
  2. 2.Marine Science LaboratoriesCentre for Applied Marine SciencesMenai Bridge, AngleseyUK
  3. 3.UMR M100 Physiologie et Ecophysiologie des Mollusques MarinsIfremerPlouzanéFrance
  4. 4.Laboratoire Génétique et PathologieIfremerLa TrembladeFrance

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